Embryo defective12 encodes the plastid initiation factor 3 and is essential for embryogenesis in maize

Plant Journal

Volumn 74, Issue 5, 2013, Pages 792-804

  Shen, Yun ^a   Li, Cuiling ^a   McCarty, Donald R ^b   Meeley, Robert ^c   Tan, Bao Cai ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF FLORIDA   (United States)

^c PIONEER HI BRED INTERNATIONAL INC   (United States)

Author keywords

Emb12; embryogenesis; endosperm; maize; translation initiation factor 3

Indexed keywords

EMB12; EMBRYOGENESIS; ENDOSPERM; INITIATION FACTORS; MAIZE;

ANIMAL CELL CULTURE; CLONING; ENCODING (SYMBOLS); PROTEINS; RNA;

GROWTH KINETICS;

INITIATION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CLASSIFICATION; ENDOSPERM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MAIZE; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYLOGENY; PLANT SEED; PLASTID; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; ENDOSPERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE INITIATION FACTORS; PHYLOGENY; PLANT PROTEINS; PLASTIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS; ZEA MAYS;

PROKARYOTA; ZEA MAYS;

EID: 84878270449     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12161     Document Type: Article

References (60)

1. Apuya, N.R., Yadegari, R., Fischer, R.L., Harada, J.J., Goldberg, R.B., (2002) RASPBERRY3 gene encodes a novel protein important for embryo development. Plant Physiol. 129, 691-705.
2. Beick, S., Schmitz-Linneweber, C., Williams-Carrier, R., Jensen, B., Barkan, A., (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol. Cell. Biol. 28, 5337-5347.
3. Bensen, R.J., Johal, G.S., Crane, V.C., Tossberg, J.T., Schnable, P.S., Meeley, R.B., Briggs, S.P., (1995) Cloning and characterization of the maize An1 gene. Plant Cell, 7, 75-84.
4. Berger, F., Grini, P.E., Schnittger, A., (2006) Endosperm: an integrator of seed growth and development. Curr. Opin. Plant Biol. 9, 664-670.
5. Bryant, N., Lloyd, J., Sweeney, C., Myouga, F., Meinke, D., (2011) Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol. 155, 1678-1689.
6. Chateigner-Boutin, A.L., Ramos-Vega, M., Guevara-Garcia, A., et al,. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 56, 590-602.
7. Christian, B.E., Spremulli, L.L., (2009) Evidence for an active role of IF3mt in the initiation of translation in mammalian mitochondria. Biochemistry, 48, 3269-3278.
8. Clark, J.K., Sheridan, W.F., (1991) Isolation and Characterization of 51 embryo-specific Mutations of Maize. Plant Cell, 3, 935-951.
9. Coe, E.H., Thompson, D., Wallbot, V., (1988) Phenotypes Mediated by the Iojap Genotype in Maize. Am. J. Bot. 75, 634-644.
10. Costa, L.M., Gutierrez-Marcos, J.F., Brutnell, T.P., Greenland, A.J., Dickinson, H.G., (2003) The globby1-1 (glo1-1) mutation disrupts nuclear and cell division in the developing maize seed causing alterations in endosperm cell fate and tissue differentiation. Development, 130, 5009-5017.
11. De Smet, I., Lau, S., Mayer, U., Jurgens, G., (2010) Embryogenesis-the humble beginnings of plant life. Plant J. 61, 959-970.
12. Ding, Y.H., Liu, N.Y., Tang, Z.S., Liu, J., Yang, W.C., (2006) Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell, 18, 815-830.
13. Doelling, J.H., Yan, N., Kurepa, J., Walker, J., Vierstra, R.D., (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J. 27, 393-405.
14. Eastmond, P.J., van Dijken, A.J., Spielman, M., Kerr, A., Tissier, A.F., Dickinson, H.G., Jones, J.D., Smeekens, S.C., Graham, I.A., (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J. 29, 225-235.
15. Emanuel, C., Weihe, A., Graner, A., Hess, W.R., Borner, T., (2004) Chloroplast development affects expression of phage-type RNA polymerases in barley leaves. Plant J. 38, 460-472.
16. Emanuelsson, O., Brunak, S., von Heijne, G., Nielsen, H., (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971.
17. Gutierrez-Marcos, J.F., Dal Pra, M., Giulini, A., et al,. (2007) empty pericarp4 encodes a mitochondrion-targeted pentatricopeptide repeat protein necessary for seed development and plant growth in maize. Plant Cell, 19, 196-210.
18. Hajdukiewicz, P.T., Allison, L.A., Maliga, P., (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16, 4041-4048.
19. Han, C.D., Coe, E.H. Jr, Martienssen, R.A., (1992) Molecular cloning and characterization of iojap (ij), a pattern striping gene of maize. EMBO J. 11, 4037-4046.
20. Haque, M.E., Spremulli, L.L., (2008) Roles of the N- and C-terminal domains of mammalian mitochondrial initiation factor 3 in protein biosynthesis. J. Mol. Biol. 384, 929-940.
21. Hsu, S.C., Belmonte, M.F., Harada, J.J., Inoue, K., (2010) Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr. Genomics, 11, 338-349.
22. Hu, G., Yalpani, N., Briggs, S.P., Johal, G.S., (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell, 10, 1095-1105.
23. Inaba, T., Ito-Inaba, Y., (2010) Versatile roles of plastids in plant growth and development. Plant Cell Physiol. 51, 1847-1853.
24. Ishikawa, A., Okamoto, H., Iwasaki, Y., Asahi, T., (2001) A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. Plant J. 27, 89-99.
25. Julian, P., Milon, P., Agirrezabala, X., Lasso, G., Gil, D., Rodnina, M.V., Valle, M., (2011) The Cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli. PLoS Biol. 9, e1001095.
26. Kondou, Y., Nakazawa, M., Kawashima, M., et al,. (2008) RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol. 147, 1924-1935.
27. Kroeger, T.S., Watkins, K.P., Friso, G., van Wijk, K.J., Barkan, A., (2009) A plant-specific RNA-binding domain revealed through analysis of chloroplast group II intron splicing. Proc Natl Acad Sci U S A, 106, 4537-4542.
28. Kuroda, H., Maliga, P., (2003) The plastid clpP1 protease gene is essential for plant development. Nature, 425, 86-89.
29. Laursen, B.S., Sorensen, H.P., Mortensen, K.K., Sperling-Petersen, H.U., (2005) Initiation of protein synthesis in bacteria. Microbiol. Mol. Biol. Rev. 69, 101-123.
30. Legen, J., Kemp, S., Krause, K., Profanter, B., Herrmann, R.G., Maier, R.M., (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J. 31, 171-188.
31. Lin, B.Y., (1984) Ploidy barrier to endosperm development in maize. Genetics, 107, 103-115.
32. Linkies, A., Graeber, K., Knight, C., Leubner-Metzger, G., (2010) The evolution of seeds. New Phytol. 186, 817-831.
33. Lisch, D., (2002) Mutator transposons. Trends Plant Sci. 7, 498-504.
34. Ma, Z., Dooner, H.K., (2004) A mutation in the nuclear-encoded plastid ribosomal protein S9 leads to early embryo lethality in maize. Plant J. 37, 92-103.
35. Maar, D., Liveris, D., Sussman, J.K., Ringquist, S., Moll, I., Heredia, N., Kil, A., Blasi, U., Schwartz, I., Simons, R.W., (2008) A single mutation in the IF3 N-terminal domain perturbs the fidelity of translation initiation at three levels. J. Mol. Biol. 383, 937-944.
36. Magnard, J.L., Heckel, T., Massonneau, A., Wisniewski, J.P., Cordelier, S., Lassagne, H., Perez, P., Dumas, C., Rogowsky, P.M., (2004) Morphogenesis of maize embryos requires ZmPRPL35-1 encoding a plastid ribosomal protein. Plant Physiol. 134, 649-663.
37. Maier, R.M., Neckermann, K., Igloi, G.L., Kossel, H., (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J. Mol. Biol. 251, 614-628.
38. McCarty, D.R., Settles, A.M., Suzuki, M., et al,. (2005) Steady-state transposon mutagenesis in inbred maize. Plant J. 44, 52-61.
39. Myers, A.M., James, M.G., Lin, Q., Yi, G., Stinard, P.S., Hennen-Bierwagen, T.A., Becraft, P.W., (2011) Maize opaque5 encodes monogalactosyldiacylglycerol synthase and specifically affects galactolipids necessary for amyloplast and chloroplast function. Plant Cell, 23, 2331-2347.
40. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., Kimura, T., (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41.
41. Neuffer, M.G., Sheridan, W.F., (1980) Defective kernel mutants of maize. I. Genetic and lethality studies. Genetics, 95, 929-944.
42. Olsen, O.A., (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell, 16 (Suppl), S214-S227.
43. Opsahl-Ferstad, H.G., Le Deunff, E., Dumas, C., Rogowsky, P.M., (1997) ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J. 12, 235-246.
44. Ostheimer, G.J., Williams-Carrier, R., Belcher, S., Osborne, E., Gierke, J., Barkan, A., (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J. 22, 3919-3929.
45. Prikryl, J., Watkins, K.P., Friso, G., van Wijk, K.J., Barkan, A., (2008) A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res. 36, 5152-5165.
46. Ramundo, S., Rahire, M., Schaad, O., Rochaix, J.D., (2013) Repression of essential chloroplast genes reveals new signaling pathways and regulatory feedback loops in chlamydomonas. Plant Cell, 25, 167-186.
47. Schmitz-Linneweber, C., Williams-Carrier, R.E., Williams-Voelker, P.M., Kroeger, T.S., Vichas, A., Barkan, A., (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell, 18, 2650-2663.
48. Serino, G., Maliga, P., (1998) RNA polymerase subunits encoded by the plastid rpo genes are not shared with the nucleus-encoded plastid enzyme. Plant Physiol. 117, 1165-1170.
49. Settles, A.M., Latshaw, S., McCarty, D.R., (2004) Molecular analysis of high-copy insertion sites in maize. Nucleic Acids Res. 32, e54.
50. Sheridan, W.F., Neuffer, M.G., (1980) Defective kernel mutants of maize II. Morphological and embryo culture studies. Genetics, 95, 945-960.
51. Sosso, D., Canut, M., Gendrot, G., Dedieu, A., Chambrier, P., Barkan, A., Consonni, G., Rogowsky, P.M., (2012) PPR8522 encodes a chloroplast-targeted pentatricopeptide repeat protein necessary for maize embryogenesis and vegetative development. J. Exp. Bot. 63, 5843-5857.
52. Springer, P.S., McCombie, W.R., Sundaresan, V., Martienssen, R.A., (1995) Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science, 268, 877-880.
53. Tan, B.C., Chen, Z., Shen, Y., Zhang, Y., Lai, J., and, Sun, S.S., (2011) Identification of an active new mutator transposable element in maize. G3 (Bethesda), 1, 293-302.
54. Uwer, U., Willmitzer, L., Altmann, T., (1998) Inactivation of a glycyl-tRNA synthetase leads to an arrest in plant embryo development. Plant Cell, 10, 1277-1294.
55. Vroemen, C.W., Mordhorst, A.P., Albrecht, C., Kwaaitaal, M.A., de Vries, S.C., (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell, 15, 1563-1577.
56. Wallace, J.C., Lopes, M.A., Paiva, E., Larkins, B.A., (1990) New methods for extraction and quantitation of zeins reveal a high content of gamma-zein in modified opaque-2 maize. Plant Physiol. 92, 191-196.
57. Weijers, D., Van Hamburg, J.P., Van Rijn, E., Hooykaas, P.J., Offringa, R., (2003) Diphtheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiol. 133, 1882-1892.
58. Williams, P.M., Barkan, A., (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36, 675-686.
59. Woodson, J.D., Perez-Ruiz, J.M., Chory, J., (2011) Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr. Biol. 21, 897-903.
60. Zhelyazkova, P., Sharma, C.M., Forstner, K.U., Liere, K., Vogel, J., Borner, T., (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell, 24, 123-136.